Differentiating genetic and environmental drivers of plant-pathogen community interactions

1. Plant genotypic variation can shape associated arthropod and microbial communities locally, as has been demonstrated in controlled common garden experiments. However, the relative roles of plant genetics and the environment in defining communities at larger spatial scales are not well known. The environmental heterogeneity hypothesis maintains that plant genetic effects on associated communities diminish across the landscape as environmental variation predominates. Alternatively, the local adaptation hypothesis argues that plant genetic effects change across landscapes as a result of species interactions being locally adapted. Thus, very different mechanisms could produce similar patterns. 2. Using replicated common gardens located along an elevation and distance gradient, observational studies in the wild, and a greenhouse inoculation experiment, we examined these two non-mutually exclusive hypotheses for Populus angustifolia and its fungal leaf pathogen community. 3. Supporting the environmental heterogeneity hypothesis, plant genotypic effects on fungal leaf pathogen communities were two to three times stronger within than among gardens. Consistent with the local adaptation hypothesis, plant genotypic effects on pathogens also varied significantly among gardens (i.e. G x E interaction effect). Observational data from the wild and our greenhouse inoculation experiment unveiled clinal adaptation in plant genetic resistance that is correlated with disease risk along the elevation gradient, but did not support local pathogen adaptation to plants or vice versa. 4. Synthesis. While our study found that plant genotype plays a significant role in shaping associated pathogen communities at local and geographic scales, the environment most strongly influenced P. angustifolia leaf pathogens at the geographic scale. Plant genetic effects on pathogens were also influenced by the environment, highlighting the potential for environmental (e.g. climate) change to trigger local evolutionary responses in plant-pathogen community interactions.